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Arch Cardiovasc Imaging. 2014 February; 2(1):e14534.
DOI: 10.5812/acvi.14534
Research Article
Published online 2014 January 12.
Echocardiographic Abnormalities in Patients with Sleep Apnea Syndrome
1
2
Maryam Moshkani Farahani, MD ; Ensieh Vahedi, MD ; Iman Lotfian, MD
4
Motashaker-Arani
3,*
; Mahdi
1Atherosclerosis Research Center, Baqiyatallah University of Medical Sciences, Tehran, IR Iran
2Chemical Injury Research Center, Baqiyatallah University of Medical Sciences, Tehran, IR Iran
3Health Research Center, Baqiyatallah University of Medical Sciences, Tehran, IR Iran
4Students Research Committee, Baqiyatallah University of Medical Sciences, Tehran, IR Iran
*Corresponding author: Iman Lotfian, MD, Health Research Center, Baqiyatallah University of Medical Sciences, Tehran, IR Iran. Tel: +98-2182482394, Fax: +98-2181263420, E-mail: iman.
[email protected]
Received: September 1, 2013; Revised: October 4, 2013; Accepted: November 17, 2013
Background: Obstructive sleep apnea (OSA) is a common sleep disease. It is associated not only with hypertension but also with other
cardiac complications. Thus, the early detection of cardiac disorders is very useful.
Objectives: We sought to evaluate different echocardiographic parameters.
Patients and Methods: This cross-sectional study was done on 55 patients with OSA. The patients were divided into three groups: mild,
moderate, and severe according to the apnea hypopnea index (AHI) and all underwent echocardiography. Analysis was done by SPSS 18 as
well as the chi-squared and one-way ANOVA tests.
Results: The mean age of the study population was 51.16 ± 12.88 years old and 36 (65.5%) patients were male. Right Tei index mean was
0.383 ± 0.213, which was abnormal in 19.1% of the patients. Left Tei index mean was 0.378 ± 0.230 and was abnormal in 52.9% of the patients.
Pulmonary artery pressure mean was 18.32 ± 8.91 and was normal in 39 (70.9%) patients. Only basal septum strain (P = 0.015) and basal
septum strain rate (P = 0.005) changes were associated with OSA severity.
Conclusions: The main findings of this study were relative left ventricular systolic and diastolic dysfunction as well as dysfunction in
some parameters of the right ventricle. The prevalence of these disorders and what constitutes the best echocardiographic parameter for
their diagnosis are controversial and require further research.
Keywords: Obstructive Sleep Apnea; Echocardiography; Cardiovascular Diseases
1. Background
Obstructive sleep apnea (OSA) is a syndrome with recurrent episodes of the obstruction of the upper airways and
subsequent decrease in arterial blood oxygen (1). OAS is
defined by apnea (complete cessation of breathing) or
hypopnea (partial cessation of breathing) more than 5
times per hour (2). The prevalence of this syndrome has
increased in recent years, and it currently affects 4-6% of
men, 2-4% of middle-aged women (3), and 0.7 to 3% of children. OAS is allied to functional and structural changes
in the heart (4, 5). Indeed, cardiovascular diseases are the
main complications of OAS (1). Although the exact mechanism of cardiovascular complications is unknown, they
seem to have a multifactorial pathogenesis. Echocardiography is the most common noninvasive imaging method
for assessing myocardial function and evaluating the effects of OSA on the heart.
2. Objectives
Given the existing controversies about systolic or dia-
stolic dysfunction in OSA patients, we sought to evaluate
cardiac function in these patients using tissue doppler
imaging (TDI), strain, strain rate, and Tei.
3. Patients and Methods
This cross-sectional study was conducted on 55 patients,
whose disease had been confirmed by a pulmonologist using polysomnography over a 24-hour period in hospital in
a sleep room. Inclusion criterion was a definite diagnosis
of OSA and exclusion criterion was central sleep apnea.
The patients were selected by using the archived records
of the sleep room and were invited for echocardiography.
The AHI, calculated by dividing the number of events by
the number of hours of sleep, is the most useful and objective way of classifying the severity of the disease (6). After
history taking and physical examination, the patients underwent echocardiography, which was performed in the
left lateral decubitus position. Images were obtained in
different views (parasternal long-axis as well as apical fourchamber, two-chamber, and three-chamber) and saved for
Implications for health policy/practice/research/medical education:
In light of the results of our study, we would recommend that strain, strain rate, tissue doppler imaging, and Tei be used for the initial screening of patients with
obstructive sleep apnea.
Copyright © 2014, Iran University of Medical Sciences. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which
permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Moshkani Farahani M et al.
later offline analysis. The machine used was VIVID 7 dimension (GE), with the M4S probe. Demographic characteristics and echocardiographic parameters were measured
and recorded in a datasheet for all the patients. The data
were saved in SPSS 18 database and were subsequently analyzed using the chi squared and one-way ANOVA statistical
tests. A P < 0.05 was considered as the significant level.
3.1. Ethical Issues
Because echocardiography is a noninvasive method, the
only ethical issue was the patients’ consent to undergo
echocardiography and this was resolved due to their voluntary participation in the study.
4. Results
In this study, 55 patients with apnea-hypopnea syndrome
were divided into three groups with mild [5 ≤ AHI < 15
(40%)], moderate [15 ≤ AHI < 30 (18.2%)], and severe OAS
[30 ≤ AHI (41%)] (6). The demographic characteristics of
the patients are depicted in Table 1. There were no statistically significant differences between the groups with
Table 1. Demographic Characteristicsa
Age, y
Male, %
BMIb, kg/m2
Mild Group
12.38 ± 48.72
63.6
66.50 ± 31.3
a Data are presented as mean ± SD.
b Abbreviation: BMI, body mass index
Moderate Group
14.46 ± 51.3
70
5.08 ± 30.88
respect to age, gender, and body mass index (BMI). Mean
AHI was 9.06 ± 3.41 for the patients with mild OSA, 21 ± 4.22
for those with moderate OSA, and 51.03 ± 21.81 for the ones
with severe OSA; total mean was 28.78 ± 4.12.
Out of the data available on 47 patients, 9 (19.1%) patients had abnormal right Tei and 38 (80.9%) had normal
right Tei (0.24). Out of 51 patients, 27 (52.9%) patients had
abnormal left Tei and 24 (47.1 %) had normal left Tei (0.34)
(Table 2). There were no significant differences between
the three groups in terms of right Tei and left Tei. Left ventricular ejection fraction (LVEF) and pulmonary artery
pressure as well as echocardiographic data related to TDI,
strain, and strain rate are given in Table 2, which shows
that only basal septal strain (P = 0.15) and basal septal
strain rate (P = 0.005) had a significant relationship with
the severity of the disease. Because of the effect of hypertension and ischemic heart disease in cardiac structure
and function, we studied the pure effect of OSA on echocardiographic variables. As is shown in Table 2, only left
strain in the patients with hypertension and/or ischemic
heart disease (P = 0.002) and left strain rate in those with
OSA and without hypertension and/or ischemic heart disease were significant.
Severe Group
12.81 ± 53.4
65.2
7.16 ± 34.56
All Groups
12.885 ± 51.16
65.5
6.676 ± 32.59
P value
0.48
0.58
0.177
Table 2. Two-Dimensional, TDI, Strain and Strain Rate Echocardiography Informationa,b
Mild Group Moderate Group Severe Group
Total
7.12 ± 1.33
5.38 ± 2.55
8.42 ± 1.46
5.90 ± 2.18
5.38 ± 3.63
8.12 ± 0.74
11.23 ± 4.18
7.42 ± 2.79
11.23 ± 4.18
0.49 ± 0.27
0.75 ± 0.54
-17.76 ± 9.40
-19.75 ± 10.78
0.400 ± 0.166
0.360 ± 0.246
52.90 ± 2.51
18.60 ± 11.10
6.26 ± 2.01
5.56 ± 2.95
7.5 ± 2.36
5.49 ± 2.22
5.63 ± 3.75
6.59 ± 2.78
9.77 ± 2.77
6.50 ± 3.17
9.39 ± 4.01
2.34 ± 4.36
1.18 ± 1.02
-17.19 ± 11.82
-16.15 ± 10.36
0.392 ± 0.208
0.387 ± 0.230
52.74 ± 3.99
18.32 ± 7.91
LV TDI BS Sm, cm/s
6.22 ± 2.30
LV TDI BS Em, cm/s
6.13 ± 3.06
LV TDI BS Am, cm/s
7.31
LV TDI BL S, cm/s
6.28 ± 2.07
LV TDI BL E, cm/s
7.34 ± 3.90
LV TDI BL A, cm/s
6.28 ± 2.07
RVTDIB LS, cm/s
8.92 ± 2.76
RVTDIB LE, cm/s
7.37 ± 3.49
RVTDIB LA, cm/s
6.37 ± 3.49
Left BS strain rate
1.78 ± 0.50
Right BL strain rate
1.30 ± 1.49
Left BS strain
24.86 ± 13.61
Right BL strain
-17.69 ± 13.09
Right Tei
0.439 ± 0.236
Left Tei
0.4011 ± 0.236
LVEF, %
52.63 ± 4.96
PAP, mm Hg
17.86 ± 5.19
5.95 ± 1.97
5.14 ± 3.08
7.43 ± 2.50
4.73 ± 2.50
4.34 ± 3.32
5.89 ± 2.83
9.75 ± 2.65
6.22 ± 3.09
9.79 ± 4.91
1.10 ± 0.68
1.25 ± 0.71
-11.04 ± 4.47
-13.86 ± 7.94
0.340 ± 0.193
0364 ± 0.257
52.78 ± 3.61
18.65 ± 10.89
P value P value HTN and/or IHD P value Only OSA
0.389
0.597
0.534
0.184
0.117
0.291
0.053
0.668
0.171
0.005
0.605
0.015
0.531
0.353
0.853
0.435
0.953
0.432
0.126
0.464
0.196
0.201
0.902
0. 358
0.219
0.456
0.280
0.617
0.002
0.280
0.397
0.863
0.479
0.363
0.254
0.293
0.835
0.743
0.501
0.573
0.199
0.184
0.137
0.006
0.196
0.749
0.472
0.716
0.569
0.634
0.309
a Data are presented as mean ± SD
b Abbreviations: AI, aortic insufficiency, Am, Aˊwave by tissue doppler; BL, basal lateral; BS, basal septal; Em, Eˊ wave by tissue doppler; L, Lateral; LV, left
ventricular; LVEF, left ventricular ejection fraction; PAP, pulmonary artery pressure; RVTDIB, right ventricle tissue doppler of base of lateral RV wall; S,
strain; Sm, Sˊwave by tissue doppler; SI, strain imaging; TDI, tissue doppler imaging
2
Arch Cardiovasc Imaging. 2014;2(1):e14534
Moshkani Farahani M et al.
5. Discussion
The main findings of this study are relative LV systolic
and diastolic dysfunction as well as disorders of some
right ventricular (RV) parameters. Research shows that obstructive sleep apnea-hypopnea syndrome (OSAHS) results
in LV diastolic dysfunction before the appearance of clinical symptoms and morphological changes (1, 7-9). Hypoxic
episodes during OSAHS can increase the O2 demand of
the myocardium and this in turn results in ischemia and
subclinical LV systolic dysfunction (1). Presence or lack of
LV systolic dysfunction due to OSAHS is disputed (7, 8, 10).
This is the issue with RV function too, and the results of the
previous studies on the effect of OSAHS on RV function are
contradictory (2). In a study by BM Sanner (11), RV dysfunction was detected by using radionuclide ventriculography,
after adjusting a large number of variables. There is currently disagreement on whether or not OSAHS independently affects cardiac function (7, 10). Among the reasons
for these disagreements are the existence of some concurrent diseases such as hypertension, diabetes mellitus,
chronic obstructive pulmonary disease, ischemic heart
disease, and myocardial infarction, each of which can independently affect the function of the heart. Be that as it
may, these concurrent diseases have been omitted in some
studies (2). Another reason for such discordance in results
is the employment of dissimilar methods by different
studies. For example, while some studies have used only
two-dimensional (2D) echocardiography and Doppler (12),
others have utilized DTI and 2D-speckle tracking echocardiography. The next issue is the different parts on which
the researchers have focused. Indeed, different studies
have been performed on the apex fibers of the septum and
the lateral wall, and because these parts are affected with
different degrees, the results would be different too.
A large number of studies have confirmed that OSAHS
exerts no effect on LVEF owing to the fact the lateral fibers
grow without change in the circular fibers in early stages
of the disease and compensation of longitudinal fibers
preserves LVEF. In advanced stages of the disease, the dysfunction is evident due to the involvement of all fibers.
Some studies have reported a significant drop in LVEF in
severe disease (10, 12). In our study, LVEF in 36.4% of the patients was lower than the normal level. We evaluated strain
and strain rate for the longitudinal fibers of basal septum
and right side basal lateral (RV free wall) longitudinal fibers. Septum dysfunction was more than the right side,
and it had a significant relation with the intensity of the
disease. The advantage of evaluating the longitudinal fibers is that they are the most vulnerable fibers due to their
position in the subendocardium and their evaluation help
earlier detection of myocardial dysfunction (1). Many studies, similar to the present study, have reported dysfunction
in left strain and left strain rate with a significant correlation with disease severity (1, 4, 13). In one study, thinner and
more trabecula fibers in the apical RV were more sensitive
Arch Cardiovasc Imaging. 2014;2(1):e14534
to stress compared to the basal part (14). Accordingly, the
changes in the basal fibers are diagnosed in later stages of
the disease, and this may be a reason for the relative normal value of these criteria in our study.
TDI has been utilized more commonly in recent years
because it confers a better diagnosis of the abnormalities of the myocardium in OSAHS. Based on some studies,
however, the limitations of TDI are its load and angle dependency (15). In various studies, changes in these criteria
are subject to disagreement and conflict (9, 10, 14, 16). Tei
or myocardial performance index (MPI) is a simple, noninvasive, repeatable and functional index for assessing the
global function of the heart. As systolic dysfunction and
diastolic dysfunction of the heart are usually concurrent,
these criteria are drawn upon frequently for assessing patients with OSAHS (10, 17). In some studies, Tei is disrupted
in OSA patients (13, 18-20). Our results demonstrated relative disruption in Tei: right Tei was abnormal in 19.1% of
our patients, which was irrelevant to the severity of the
disease. (There was no significant difference between the
groups and we recommend further studies in the Iranian
population with OSA.) Various studies have reported pulmonary artery hypertension in OSA patients (15). It seems
that, with the effects of OSAHS on the pulmonary system as
a result of frequent hypoxia and hypercapnia, the changes
in pulmonary pressure are unavoidable. In a series of studies, pulmonary artery pressure was reported borderline
normal and it had no significant relationship with the
severity of the disease (4, 12). The direct effect of OSAHS
should be studied independently from the effect of other
diseases on pulmonary artery pressure. We did not detect
a significant rise in the pulmonary artery pressure of our
study population. Although the presence of pulmonary
artery hypertension is not characteristic of patients with
OSA, one explanation is the beginning of treatment for the
patients by our pulmonologist.
The following points should be taken into consideration
in the interpretation of the results of the present study:
The criterion for omitting patients from the study was
only the existence of central sleep apnea and the individuals affected with chronic obstructive pulmonary disease,
diabetes mellitus, cerebrovascular accident, ischemic
heart disease, and hypertension were entered in the study.
However, the existence of these criteria somewhat precludes the generalization of the results to the whole population (15).
We did not study the heart apex and only studied the
longitudinal fibers, which are of course the most sensitive
fibers.
Finally, we did not know the duration of the affliction of
OSA patients with or without treatment, and these different durations may be associated with different effects (10).
The principal finding of the present study was dysfunction in criteria in both ventricles, especially the left ventricle. Apart from the effects of concurrent diseases, it has
been proved that OSAHS alone affects cardiovascular func3
Moshkani Farahani M et al.
tion. Therefore, early diagnosis of this dysfunction can be
very helpful in slowing the progression of these complications. Further research with larger study populations, control groups, and more exclusion criteria is required to shed
sufficient light on this issue. Moreover, transesophageal
echocardiography (TEE) can be used for patients with poor
echo window who have high levels of BMI if they could
tolerate it. As the apical part is more sensitive, we would
recommend that strain rate, strain, and TDI be studied in
all segments. Finally, other methods for investigating the
structure and function of the heart such as magnetic resonance imaging (MRI) can be used for comparison.
5.1. Recommendations
We would recommend that strain, strain rate, TDI, and
Tei be used for the initial evaluation of these patients and
that the relationship between echocardiographic criteria
and clinical symptoms be explored in further studies.
2.
3.
4.
5.
6.
7.
5.2. Limitations
8.
First and foremost among the limitations of the present
study was the absence of the follow-up of the study population due to incorrect telephone numbers and considerable distance between the patients' place of residence
and our hospital.
9.
10.
Acknowledgements
11.
Special thanks are due to the echocardiography personnel of our hospital, Miss Sharifi, Miss Ahmadipour, Miss
Arezoo, and Miss Mousavi.
12.
Authors’ Contribution
Maryam Moshkani Farahani: Conceived and designed
the study, collected the data, and read and approved the
final version. Ensie Vahedi: Conceived and designed the
study, interpreted the data, and read and approved the final version. Iman Lotfan: Designed the study, collected the
data, drafted the manuscript, critically revised the manuscript for intellectual content, and read and approved the
final version. Mahdi Motashaker-Arai: Conducted statistical analysis, analyzed and interpreted the data, drafted the
manuscript, and read and approved the final version.
Financial Disclosure
There are no financial interests related to the material
in the manuscript.
Funding/Support
We had no financial support from any organization or
department.
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